nutrients

Article
Percentage of Body Fat and Fat Mass Index
as a Screening Tool for Metabolic Syndrome
Prediction in Colombian University Students
Robinson Ramrez-Vlez 1, * ID , Jorge Enrique Correa-Bautista 1 ID ,
Alejandra Sanders-Tordecilla 1 , Mnica Liliana Ojeda-Pardo 2 , Elisa Andrea Cobo-Meja 2 ,
Roco del Pilar Castellanos-Vega 2 , Antonio Garca-Hermoso 3 ID , Emilio Gonzlez-Jimnez 4,5 ID
,
Jacqueline Schmidt-RioValle 4,5 and Katherine Gonzlez-Ruz 6
1 Centro de Estudios para la Medicin de la Actividad Fsica CEMA, Escuela de Medicina y Ciencias de la
Salud, Universidad del Rosario, Bogot DC 111221, Colombia; jorge.correa@urosario.edu.co (J.E.C.-B.);
alesanders_0615@hotmail.com (A.S.-T.)
2 Grupo CORPS, Universidad de Boyac, Facultad de Ciencias de la Salud, Boyac 150003, Colombia;
mlojeda@uniboyaca.edu.co (M.L.O.-P.); eacobo@uniboyaca.edu.co (E.A.C.-M.);
dpcastellanos@uniboyaca.edu.co (R.d.P.C.-V.)
3 Laboratorio de Ciencias de la Actividad Fsica, el Deporte y la Salud, Facultad de Ciencias Mdicas,
Universidad de Santiago de Chile, USACH, Santiago 7500618, Chile; antonio.garcia.h@usach.cl
4 Departamento de Enfermera, Facultad de Ciencias de la Salud, Avda. De la Ilustracin, 60,
University of Granada, 18016 Granada, Spain; emigoji@ugr.es (E.G.-J.); jschmidt@ugr.es (J.S.-R.)
5 Grupo CTS-436, Adscrito al Centro de Investigacin Mente, Cerebro y Comportamiento (CIMCYC),
University of Granada, 18071 Granada, Spain
6 Grupo de Ejercicio Fsico y Deportes, Vicerrectora de Investigaciones, Universidad Manuela Beltrn,
Bogot DC 110231, Colombia; katherine.gonzalez@docentes.umb.edu.co
* Correspondence: robin640@hotmail.com or robinson.ramirez@urosario.edu.co;
Tel.: +57-1-297-0200 (ext. 3428)

Received: 26 June 2017; Accepted: 11 September 2017; Published: 13 September 2017

Abstract: High body fat is related to metabolic syndrome (MetS) in all ethnic groups. Based on
the International Diabetes Federation (IDF) definition of MetS, the aim of this study was to
explore thresholds of body fat percentage (BF%) and fat mass index (FMI) for the prediction
of MetS among Colombian University students. A cross-sectional study was conducted on
1687 volunteers (63.4% women, mean age = 20.6 years). Weight, waist circumference, serum lipids
indices, blood pressure, and fasting plasma glucose were measured. Body composition was
measured by bioelectrical impedance analysis (BIA) and FMI was calculated. MetS was defined as
including more than or equal to three of the metabolic abnormalities according to the IDF definition.
Receiver operating curve (ROC) analysis was used to determine optimal cut-off points for BF% and
FMI in relation to the area under the curve (AUC), sensitivity, and specificity in both sexes. The overall
prevalence of MetS was found to be 7.7%, higher in men than women (11.1% vs. 5.3%; p < 0.001).
BF% and FMI were positively correlated to MetS components (p < 0.05). ROC analysis indicated
that BF% and FMI can be used with moderate accuracy to identify MetS in university-aged students.
BF% and FMI thresholds of 25.55% and 6.97 kg/m2 in men, and 38.95% and 11.86 kg/m2 in women,
were found to be indicative of high MetS risk. Based on the IDF criteria, both indexes thresholds
seem to be good tools to identify university students with unfavorable metabolic profiles.

Keywords: obesity; adiposity; fat mass; metabolic syndrome

Nutrients 2017, 9, 1009; doi:10.3390/nu9091009 www.mdpi.com/journal/nutrients

Nutrients 2017, 9, 1009 2 of 13

1. Introduction
With increasing prevalence worldwide, obesity has become a significant public health issue [1].
Obesity has been linked to a number of cardiovascular disease (CVD) risk factors including metabolic
syndrome (MetS) [2]. In Colombia, it is estimated that over 50% of adults are overweight or obese and
the obesity epidemic has been associated with obesogenic factors, such as an intake of energy-dense
diets, a sedentary lifestyle, and low levels of physical activity [3,4] .
In this context, there is growing evidence that suggests that the way in which fat is distributed
contributes different effects on the cardiometabolic risk associated with obesity [35]. In addition,
measures of central body obesity, such as waist circumference and waisthip ratio, have been
suggested as being more strongly related to MetS risk compared to body mass index (BMI) [4,5].
Aside from age or sex, excess body fat is the strongest determinant of an individuals risk of developing
MetS [6], and several epidemiological studies have found an association between fat distribution and
metabolic risk factors, including high blood pressure, dysglycemia, dyslipidemia, and subsequent risk
of MetS [4,5].
Although BMI is the most frequently used method to assess the level of obesity [7], BMI does not
differentiate between body lean mass and body fat mass; that is, a person can have a high BMI but still
have a low fat mass and vice versa [8,9]. In addition, the ongoing uncertainty as to which measure
of body fat is most important at gauging an individuals risk [6], particularly with respect to MetS,
may also contribute to the lack of their use and monitoring in clinical practice.
In this sense, Computed Tomography (CT) or dual-energy X-ray absorptiometry (DXA),
continue to be the gold standard for evaluating the distribution of body fat [10]. Nevertheless,
the high cost and low availability have made it difficult to use in large population studies. Evidently,
this factor limits the possible screening of MetS in high-risk populations, especially in developing
countries such as Colombia [2,11]. Recently, more research has examined the potential role of body
composition measurements in health monitoring [12,13]. Bioelectrical impedance analysis (BIA) is the
method that is most frequently used to assess body composition and calculate BF% in clinical practice,
given its accuracy, simplicity, low cost, and excellent correlation with DXA, CT, or magnetic resonance
imaging (MRI) [14,15].
Alternative simple and inexpensive approaches for assessing body adiposity have been suggested.
A recent study highlighted the usefulness of the fat mass index (FMI), measured as kg/m2 ,
as an indicator of the function of adipose tissue as a surrogate marker of cardiovascular risk in young
adults [16]. However, BF% and FFM are known to change with height, weight, sex, and age. Along this
line, VanItallie et al. [16] proposed an FMI that considers an individuals height. FMI, like BMI
except that it uses a two-compartment model, merits reappraisal and appears to be of interest in the
classification of overweight, obese, and underweight patients [17]. Previous research has evaluated
the applicability of FMI in the prediction of MetS and has highlighted its close relation with the
components of MetS [17]. However, only a few studies have focused on the differential impacts
adiposity levels [1824] in young adults when examining the link between fat and the risk of MetS.
Understanding the specific fat distribution associated with MetS risk is important to improve
the interventions that are currently more focused on overall weight loss [5,6]. Our study proposes
a gender-specific fat index based on BIA as a way of estimating the fat mass and body adiposity
dysfunction associated with MetS. Apart from the study of Liu et al. [17], this is the first study in
Colombian young adults (university students) to investigate the association between fat mass by BIA
and MetS components. Based on the IDF definition of MetS [2], the aim of the study was to explore
thresholds of BF% and FMI for the prediction of MetS among Colombian university students.
Nutrients 2017, 9, 1009 3 of 13

2. Methods

2.1. Study Design and Sample Population

During the 20142017 academic years, we reviewed a cross-sectional component of the FUPRECOL
study that investigated the association between muscular strength and metabolic risk factors in
Colombian collegiate students. The FUPRECOL study aimed to establish the general prevalence
of cardiovascular risk factors, including anthropometric and metabolic markers, in the study
population and to examine the relationships between physical fitness levels, body composition,
and cardiometabolic risk factors. We recently published a complete description of the FUPRECOL
study design, methods, and primary outcomes for our current cohort [2]. The sample consisted
of adults (men: n = 707; women: n = 1128). We removed cases due to missing (n = 37, 2.0%) or
erroneous data entry (n = 83, 4.5%) and those which had neither age nor a valid date of birth recorded
(n = 28, 1.5%), limiting the analytical sample to 1687 volunteers, which was 63.4% women and
a mean age of 20.6 years. The subjects, whose ages ranged from 18 to 35 years, were all of low to
middle socioeconomic status (SISBEN levels: 14 on a scale of 16 as defined by The System of
Identifying Potential Beneficiaries of Social Programs, called SISBEN). The system takes into account
sociodemographic characteristics including family composition, employment status, family income,
and educational level; living conditions, including construction type and materials; and access to
public utilities, which involves sewers, electricity, potable water, and garbage collection. They were
enrolled in public or private universities in the capital district of Bogota, Boyac, and Cali, Colombia.
Exclusion criteria included the following: medical or clinical diagnosis of a major systemic
disease including malignant conditions such as cancer, type 1 or 2 diabetes, high blood pressure,
hypothyroidism or hyperthyroidism; a history of drug or alcohol abuse; regular use of multivitamins;
chronic inflammatory conditions including rheumatoid arthritis, systemic lupus erythematosus,
multiple sclerosis; infectious conditions; and a BMI 35 kg/m2 . Volunteers received no compensation
for their participation.

2.2. Data Collection

Subjects were screened for inclusion in the study via personal interviews. Interview questions
collected consisted of health status, medical history, CVD risk factors, and lifestyle. After completing
another general information questionnaire, participants were instructed to wear shorts and a T-shirt
to the physical exam. They were also required to remove all worn jewelry and metal objects.
Once the subjects were barefoot and in their underwear, their body weight (kg) was measured using
an electric scale (Model Tanita BC-418 , Tokyo, Japan) with a range of 0200 kg and with an accuracy
of within 100 g. Height was measured with a portable stadiometer with a precision of 0.1 cm and a range
of 02.5 m (Seca 274, Hamburg, Germany). BMI was calculated by using the formula proposed by
Quetelet where BMI = body mass (kg)/height (m2 ). Body mass index status was evaluated according to
the World Health Organization (WHO) criteria [24]. The waist circumference (WC) (cm) was measured
as the narrowest point between the lower costal border and the iliac crest. When this point was not
evident, it was measured at the midpoint between the last rib and the iliac crest, using a metal tape
measure (Lufkin W606PM , Parsippany, NJ, USA), in accordance with the International Society for
the Advancement of Kinanthropometry guidelines [25]. The evaluation process was carried out by
a team of professionals (four physical therapy professors) with extensive experience in anthropometric
measurement. Two percent of the sample was measured twice in order to ensure quality of measures.
The technical error of measurement (TEM) values was less than 2% for all anthropometric variables.
BF% and FMI were determined for BIA by a tetrapolar whole body impedance (Tanita Model
BC-418 , Tokyo, Japan). A detailed description of the BIA technique can be found in a previous
study [2]. For the calculation of intrainter observer TEM, at least 50 subjects needed to be measured
(30 men, 20 women, aged 22.3 2.1 years). The corresponding intra-observer technical error
(% reliability) of the measurements was 95%. FMI was then calculated by dividing each subjects fat
Nutrients 2017, 9, 1009 4 of 13

mass (kg) by the square of his or her height (m), as previously described [17]. In a sub-sample (48 adults,
54% women, range mean age = 20 to 40 years old), we verified the validity of BIA for predicting BF%
in Colombian adults using DXA as a reference. Our analysis showed a strong agreement between
the two methods, as reflected in the range of BF% (Lins concordance correlation coefficient = 0.943
(95% CI = 0.775 to 0.950, p = 0.041) and bias 0.6 (SD 2.2; 95% CI = 5.0 to 3.7). In line with our
findings, a previously study has shown a high correlation between fat mass determined by BIA and
that obtained by a CT scan and DXA [14,15,26]. Thus, these results show that BIA and DXA are
comparable methods for measuring body composition with lower/higher body fat percentages.

2.3. Metabolic Syndrome Diagnosis

After the subjects had fasted for 1012 h, blood samples were obtained from capillary sampling
between 6:00 a.m. and 9:00 a.m. Participants were asked not to engage in prolonged exercise in the 24 h
prior to testing. The biochemical profile included the following: (i) high-density lipoprotein cholesterol
(HDL-C); (ii) triglycerides; (iii) low-density lipoprotein cholesterol (LDL-C); (iv) total cholesterol;
(v) glucose fasting by enzymatic colorimetric methods (CardioChek PA , Polymer Technology Systems,
PTS, Indianapolis, IN, USA). The inter-assay reproducibility (coefficient of variation) was determined
from 16 replicate analyses of 8 capillary blood pools over a period of 15 days. The percentages obtained
were 2.6% for triglycerides, 2.0% for total cholesterol, 3.2% for HDL-C, 3.6% for LDL-C, and 1.5% for
fasting glucose.
Blood pressure was taken on the left arm at the heart level with an automatic device Omron M6
Comfort (Omron Healthcare Europe B.V., Hoofddorp, The Netherlands) while the participants were
sitting still. The blood pressure monitor cuff was placed two to three finger-widths above the bend
of the arm and a two-minute pause was allowed between the first and second measurements with
a standard cuff for an arm circumference of 2232 cm.
MetS was defined in accordance with the updated harmonized criteria of the IDF [2]. Participants
were considered to have MetS if they showed three or more of the following: (1) abdominal obesity for
individuals (WC 80 cm in women and 90 cm in men) [27]; (2) hypertriglyceridemia (150 g/dL);
(3) low HDL-C (<50 mg/dL in women and <40 mg/dL in men); (4) high blood pressure (systolic blood
pressure 130 mmHg or diastolic blood pressure 85 mmHg); (5) high fasting glucose (100 mg/dL).

2.4. Lifestyle Co-Variables

A standardized questionnaire, FANTASTIC lifestyle, was used to collect comprehensive
information about substance use via a personal interview with participants [28]. Alcohol consumption
and smoking status were defined as subjects who had consumed any alcoholic beverage 1 times
per week, and those who had smoked 10 cigarettes per week, for at least six months, as previously
described by Ramrez-Vlez et al. [28]. Participants who exercised three or more times a week
for >30 min were categorized as physically active (PA), and those who exercised less than three
times a week were considered insufficiently physically active. The accuracy of information about
lifestyle co-variables obtained from the FANTASTIC questionnaire has been validated by different
cross-sectional studies and described in detail elsewhere [28,29].

2.5. Ethics Statement

Informed consent was obtained from each participant. The protocol was based on the Helsinki
Declaration Accord (World Medical Association for Human Subjects). Moreover, ethical approval was
obtained from the Universidad Manuela Beltrn (UMB N 01-1802-2013).

2.6. Statistical Analysis

Participants characteristics obtained were given as mean values and standard deviation (SD).
Histograms and QQ plots were used to verify the normality of the selected variables. Independent
two-tailed t-tests for continuous variables, and chi-square (2 ) tests for categorical variables, were used
Nutrients 2017, 9, 1009 5 of 13

to examine sex differences or MetS grouping. The relationships between BF%, FMI, and MetS
components were tested by means of partial correlation coefficients. This analysis was adjusted by age,
sex, tobacco, and alcohol consumption, and PA levels. To predict MetS with BF% and FMI, we used area
under the curve (AUC), ranging between 0 and 1 (a worthless and a perfect test, respectively), which is
a global indicator of diagnostic performance, and represents the ability of the test to correctly classify
participants with high risk MetS by p-values < 0.01 and an AUC > 0.80. The positive likelihood ratio
LR (+) and the negative likelihood ratio LR () were also determined. Cutoff points were chosen based
on the highest Youden index, i.e., the point on the receiver operating characteristic curve (ROC) that is
farthest from the line of equality [30]. Data analysis was performed using the Statistical Package for the
Social Sciences for Windows SPSS, version 21.0 (SPSS Inc., Chicago, IL, USA). Statistical significance
was set at p < 0.05.

3. Results

3.1. Descriptive Characteristics

Descriptive characteristics of the participants are presented in Table 1. The final sample had
a mean age of 20.6 years (SD 3.0; range 1924 years), with 63.4% of participants being women. Women
were found to have significantly lower height, WC, blood pressure, triglycerides, and PA than men
(p < 0.05). The prevalence of MetS was higher in men than in women at 11.2% vs. 5.3% (p < 0.001).

Table 1. Characteristics among a sample of college students from Colombia (mean (SD) or frequency (%)).

Characteristic Men (n = 617) Women (n = 1070) p-Value

Anthropometric
Age (years) 20.6 (2.2) 20.6 (2.0) 0.843
Weight (kg) 58.9 (10.0) 69.9 (12.4) <0.001
Height (cm) 159.8 (6.1) 172.5 (6.7) <0.001
WC (cm) 78.4 (9.5) 71.5 (7.9) <0.001
BMI (kg/m2 ) 23.2 (3.7) 23.2 (3.7) 0.356
Body fat (%) 15.7 (6.7) 27.0 (7.2) 0.028
FMI 3.9 (2.3) 6.5 (2.7) <0.001
Body mass index status n (%) *
Underweight 34 (5.5) 71 (6.7)
Normal weight 425 (68.8) 725 (57.8)
<0.001
Overweight 128 (20.8) 220 (20.5)
Obese 31 (5.0) 54 (5.0)
Blood pressure
Systolic blood pressure (mmHg) 120.83 (13.0) 111.28 (11.1) <0.001
Diastolic blood pressure (mmHg) 74.83 (11.4) 71.78 (9.3) <0.001
Mean arterial pressure (mmHg) 97.83 (10.8) 91.53 (8.9) <0.001
Metabolic biomarkers
Total cholesterol (mg/dL) 132.26 (30.8) 146.27 (33.3) 0.212
Triglycerides (mg/dL) 93.01 (48.7) 88.10 (43.7) 0.011
LDL-C (mg/dL) 38.92 (10.4) 43.98 (12.8) <0.001
HDL-C (mg/dL) 81.89 (26.5) 87.85 (26.2) 0.589
Glucose (mg/dL) 84.36 (12.2) 85.99 (11.6) 0.002
Metabolic Syndrome n (%) *
Yes 73 (11.2) 59 (5.3) 0.001
Life-style n (%) *
Tobacco (10 cigarettes per week) 183 (29.7) 213 (19.9) 0.289
Alcohol (1 times per week) 294 (47.6) 381 (35.6) 0.358
PA (three or more times a week for >30 min) 213 (34.5) 228 (21.3) 0.011
Continuous variables are reported as mean values (standard deviations) and categorical variables are reported
as numbers and percentages in brackets. Significant between-sex differences (t-tests or * chi-square test 2 ).
WC: waist circumference; BMI: body mass index; FMI: fat mass index; LDL-C: low-density lipoprotein cholesterol;
HDL-C: high-density lipoprotein cholesterol; PA: physical activity.
Nutrients 2017, 9, 1009 6 of 13

At least one MetS component was found in 818 participants (48.5%), two MetS components were
present in 341 participants (20.2%), three MetS components were found in 126 participants (7.7%),
and four or more
Nutrientscomponents
2017, 9, 1009 of MetS were present in 80 participants (4.7%) (Figure61).
of 13

Figure 1. Distribution of the prevalence of metabolic syndrome components according to sex.

Figure 1. Distribution of the prevalence of metabolic syndrome components according to sex.
3.2. Clinical Characteristics and Distribution by MetS Status
3.2. Clinical Characteristics
Independent and Distribution
of sex, by MetS
participants with Status
MetS had significantly higher weight, body mass index,
WC, BF%, FMI, and total cholesterol and triglyceride levels (p < 0.01) (Table 2). Furthermore,
Independent of sex,
participants participants
without MetS were with MetS(34.5%
more active had vs.significantly
17.8% for men,higher weight,
and 21.1% vs. 6.8%body mass index, WC,
for women,
BF%, FMI, and total cholesterol and triglyceride levels (p < 0.01) (Table 2). Furthermore, participants
p < 0.01).
without MetS were Table
more2. The
active (34.5% vs. 17.8% for men, and 21.1% vs. 6.8% for women, p < 0.01).
descriptive characteristics of participants with and without MetS in both sexes.
Men (n = 617) Women (n = 1070)
Table 2. The descriptive
Variable characteristics of participants
MetS Non-MetS with andMetS
p Value
without MetS in
Non-MetS both sexes.
p Value
(n = 73) (n = 544) (n = 59) (n = 1011)
Anthropometric
Age (years) Men (n =20.4
21.7 (3.4) 617)(3.1) 0.229 22.3 (3.8) 20.5 (2.8) Women (n = 1070)
<0.001
Weight (kg) 80.8 (15.8) 67.3 (10.7) <0.001 76.4 (13.8) 57.4 (8.8) <0.001
Variable MetS 172.7 (7.5) Non-MetS MetS Non-MetS
Height (cm) 172.1 (6.6) 0.129
p Value 161.1 (5.6) 158.9 (5.8) 0.902 p Value
WC (cm) (n = 73) 89.5 (11.6) (n =76.7 544)(8.0) <0.001 84.9 (8.8) (n =70.5
59)(7.1) (n = 1011)
0.145
BMI (kg/m2) 27.0 (4.7) 22.6 (3.1) <0.001 29.3 (4.7) 22.7 (3.3) <0.001
Anthropometric
Body fat (%) 23.5 (7.5) 14.5 (5.7) 0.005 37.3 (6.0) 26.2 (6.8) <0.001
Age (years) 21.7 (3.4) 20.4 (3.1) 0.229 22.3 (3.8) 20.5 (2.8) <0.001
FMI (kg/m2) 6.6 (3.1) 3.4 (1.8) <0.001 11.2 (3.4) 6.1 (2.4) <0.001
Weight (kg) Body mass index status n (%)80.8*
(15.8) 67.3 (10.7) <0.001 76.4 (13.8) 57.4 (8.8) <0.001
Height (cm) Underweight 172.7 (7.5) 4 (0.6) 172.130(6.6) (5.0) 0.129 0.0 (0.0) 161.1 (5.6)
71 (6.6) 158.9 (5.8) 0.902
WC (cm) Normal weight 89.5 (11.6) 16 (2.6) 76.7408 (8.0)
(66.1) <0.001 8 (0.8) 84.9 717
(8.8)
(67.0) 70.5 (7.1) 0.145
2 <0.001 <0.001
BMI (kg/m ) Overweight 27.0 (4.7) 37 (6.0) 22.691 (3.1)
(14.8) <0.001 23 (2.1) 29.3 197
(4.7)
(18.4) 22.7 (3.3) <0.001
Body fat (%) Obese 23.5 (7.5) 16 (2.6) 14.5 15 (2.4)
(5.7) 0.005 28 (2.6) 26 (2.4)
37.3 (6.0) 26.2 (6.8) <0.001
FMI (kg/m )2 Blood pressure 6.6 (3.1) 3.4 (1.8) <0.001 11.2 (3.4) 6.1 (2.4) <0.001
Systolic blood pressure (mmHg) 131.01 (11.96) 119.36 (12.44) 0.461 123.50 (11.03) 110.33 (10.64) 0.809
Body mass index status n (%)
Diastolic * pressure (mmHg)
blood 83.60 (10.75) 73.48 (10.07) 0.160 81.61 (13.82) 71.10 (8.60) 0.237
UnderweightMean blood pressure (mmHg) 4 (0.6) 107.30 (10.20) 3096.42 (5.0)(10.07) 0.176 102.55 (9.16) 0.0 90.71
(0.0)(8.36) 0.51871(6.6)
Normal weight Metabolic biomarkers 16 (2.6) 408 (66.1) 8 (0.8) 717 (67.0)
Total cholesterol (mg/dL) 146.01 (39.6) <0.001153.39 (33.7) <0.001
Overweight 37 (6.0) 91 (14.8)(29.1)
130.27 <0.001 23 145.74
(2.1) (33.3) 0.955
197 (18.4)
Triglyceride (mg/dL)
Obese 16 (2.6) 163.03 (75.9) 1583.04 (2.4)(33.7) <0.001 139.83 (66.6) 84.90 (40.2)
28 (2.6) <0.001
26 (2.4)
HDL-C (mg/dL) 31.27 (5.9) 40.06 (10.5) <0.001 36.51 (9.0) 44.52 (12.9) 0.002
Blood pressure LDL-C (mg/dL) 86.01 (30.8) 81.31 (26.0) 0.077 89.61 (28.4) 87.57 (26.1) 0.571
Systolic blood pressure (mmHg) Glucose (mg/dL) 131.01 (11.96) 92.44 (13.8)119.36 83.14 (11.6)
(12.44) 0.063
0.461 92.58 (14.4)
123.5085.49 (11.3)
(11.03) 0.142
110.33 (10.64) 0.809
Diastolic blood pressure (mmHg) Life-style n (%) * 83.60 (10.75) 73.48 (10.07) 0.160 81.61 (13.82) 71.10 (8.60) 0.237
Mean blood pressureTobacco
(mmHg) (10 cigarettes per week)
107.30 (10.20)19 (26.0) 96.42 155 (28.5)
(10.07) 0.769
0.176 5 (8.5) 102.55198 (19.6)
(9.16) 0.088
90.71(8.36) 0.518
Alcohol (1 times per week) 36 (49.3) 294 (54.0) 0.563 22 (37.3) 394 (38.7) 0.378
Metabolic biomarkers
PA (three or more times a week for >30 min) 13 (17.81) 188 (34.5) 0.005 4 (6.8) 213 (21.0) 0.018
Total cholesterol (mg/dL) variables are 146.01
Continuous reported(39.6) 130.27(standard
as mean values (29.1) <0.001 and categorical
deviations) 153.39 (33.7)variables145.74
are (33.3) 0.955
Triglyceride (mg/dL) 163.03 (75.9) 83.04 (33.7) <0.001 139.83 (66.6) 84.90 (40.2) <0.001
reported as numbers (percentages). Significant between-sex differences (t-tests or * chi-square test 2).
HDL-C (mg/dL) 31.27 (5.9) 40.06 (10.5) <0.001 36.51 (9.0) 44.52 (12.9) 0.002
WC: waist circumference; BMI:
LDL-C (mg/dL) 86.01 body
(30.8)mass index; FMI:
81.31 fat mass index;
(26.0) 0.077LDL-C: low-density
89.61 (28.4) lipoprotein
87.57 (26.1) 0.571
cholesterol;
Glucose (mg/dL) HDL-C: high-density lipoprotein
92.44 (13.8) cholesterol;
83.14 (11.6) PA: physical
0.063 activity. The
92.58 (14.4) mean blood
85.49 (11.3) 0.142
Life-style n (%) *
Tobacco (10 cigarettes per week) 19 (26.0) 155 (28.5) 0.769 5 (8.5) 198 (19.6) 0.088
Alcohol (1 times per week) 36 (49.3) 294 (54.0) 0.563 22 (37.3) 394 (38.7) 0.378
PA (three or more times a week for >30 min) 13 (17.81) 188 (34.5) 0.005 4 (6.8) 213 (21.0) 0.018
Continuous variables are reported as mean values (standard deviations) and categorical variables are reported as
numbers (percentages). Significant between-sex differences (t-tests or * chi-square test 2 ). WC: waist circumference;
BMI: body mass index; FMI: fat mass index; LDL-C: low-density lipoprotein cholesterol; HDL-C: high-density
lipoprotein cholesterol; PA: physical activity. The mean blood pressure was calculated using the following formula:
(systolic blood pressure + (2 diastolic blood pressure))/3.
Nutrients 2017, 9, 1009 7 of 13

Table 3 shows the partial correlation between BF%, FMI, and MetS components. Overall, BF% and
FMI were weakly positively correlated with all MetS parameters (all p < 0.05), except HDL, which was
negatively correlated.

Table 3. Results of the partial correlation analysis between body fat percentage (BF%), fat mass index
(FMI), and MetS components.

Glucose HDL-C Triglycerides Total Cholesterol MAP FMI

Variable WC (cm)
(mg/dL) (mg/dL) (mg/dL) (mg/dL) (mmHg) (kg/m2 )
Body fat (%) 0.188 * 0.239 ** 0.230 ** 0.279 ** 0.276 ** 0.827 ** 0.960 **
FMI (kg/m2 ) 0.113 ** 0.256 ** 0.230 ** 0.162 * 0.272 ** 0.860 ** 1
WC (cm) 0.106 * 0.219 0.248 0.858 ** 0.271 ** 1
Mean blood pressure (mmHg) 0.004 0.022 ** 0.179 ** 0.259 ** 1
Total cholesterol (mg/dL) 0.008 0.341 ** 0.241 ** 1
Triglycerides (mg/dL) 0.125 ** 0.170 ** 1
HDL-C (mg/dL) 0.158 ** 1
Glucose (mg/dL) 1
Analysis adjusted by co-variables: age, sex, tobacco, alcohol, and physical activity. * p < 0.05; ** p < 0.01. WC: waist
circumference; FMI: fat mass index; HDL-C: high-density lipoprotein cholesterol; MAP: mean arterial pressure.
The mean blood pressure was calculated using the following formula: (systolic blood pressure + (2 diastolic blood
pressure))/3.

3.3. Optimal Cut-Off Value in the Screening of MetS

The ROC analysis showed that BF% and FMI parameters could be used to detect MetS according
to the IDF criteria among Colombian university students (Table 4; Figure 2). Since multiple levels of
risk were desired, the selection of the resulting cut-off values was based on multiple combinations
of sensitivity and specificity. The focus was on higher sensitivity for the BF% and FMI thresholds in
an effort to identify the majority of cases of MetS according to the IDF criteria. In men, the cut-off point
valueNutrients
of 25.5%2017,for
9, 1009
BF% provided a sensitivity of 96.1%, an LR (+) value of 2.3, a specificity8of of 13
57.5%,
2
and an LR () value of 0.06. For FMI, the cut-off value of 6.9 kg/m provided a sensitivity of 95.8%,
Sensitivity (%) 97.4 97.6
an LR (+) value of 2.2, a specificity of 56.2%, and an LR () value of 0.07. With respect to BF% among
Specificity (%) 55.9 56.9
the women in the study population, the cut-off point LR (+)
value of 38.9%
2.2
provided 2.2
a sensitivity of 97.4%,
an LR (+) value of 2.2, a specificity of 55.9%, and an LR
LR () ( ) value of
0.04 0.04. The 0.04 curve for FMI was
ROC
also obtained, using a cut-off value of 11.8 kg/m 2 , a sensitivity of 97.6%, an LR (+) of 2.2, a specificity
AUC: area under the curve; CI: confidence interval; LR (+): positive likelihood ratio; LR (): negative
of 56.9%, likelihood
and an LR () of 0.04.
ratio.

Figure 2. ROC
Figure curves
2. ROC forfor
curves BF% and
BF% andFMI
FMIfor
for prediction ofthe
prediction of theprevalence
prevalenceof of MetS
MetS according
according to IDF
to IDF
criteria in men
criteria andand
in men women.
women.

4. Discussion
In our study, we found that the MetS prevalence was higher in men than in women (11.2% vs.
5.3%; p < 0.001), which is an intermediate value compared to those reported in local and international
studies, ranging from 2 to 13% [3133], that BF% and FMI were positively correlated to MetS
components (p < 0.05), and that the ROC analysis showed that both the BF% and FMI had a moderate
discriminatory power in the identification of MetS among Colombian university students.
Nutrients 2017, 9, 1009 8 of 13

Table 4. Parameters of the ROC curves analysis for the diagnostic performance of body fat percentage
(BF%) and fat mass index (kg/m2 ) in identifying high risk of MetS according to the IDF criteria in men
and women.

Parameter BF% FMI

AUC 0.835 0.838
95% CI 0.7790.891 0.7790.892
p value <0.001 <0.001
Cut-off 25.5 6.9
Men
Sensitivity (%) 96.1 95.8
Specificity (%) 57.5 56.2
LR (+) 2.3 2.2
LR () 0.06 0.07
High risk of MetS
AUC 0.887 0.889
95% CI 0.8420.932 0.8440.933
p value <0.001 <0.001
Cut-off 38.9 11.8
Women
Sensitivity (%) 97.4 97.6
Specificity (%) 55.9 56.9
LR (+) 2.2 2.2
LR () 0.04 0.04
AUC: area under the curve; CI: confidence interval; LR (+): positive likelihood ratio; LR (): negative likelihood ratio.

4. Discussion
In our study, we found that the MetS prevalence was higher in men than in women (11.2% vs. 5.3%;
p < 0.001), which is an intermediate value compared to those reported in local and international studies,
ranging from 2 to 13% [3133], that BF% and FMI were positively correlated to MetS components
(p < 0.05), and that the ROC analysis showed that both the BF% and FMI had a moderate discriminatory
power in the identification of MetS among Colombian university students.
The higher prevalence of MetS, at 11.2%, seen in male subjects in our results does not coincide
with Ruano-Nieto et al. [34] who found that the estimated prevalence of MetS was 8.4% for women
and 6.1% for men in a population of Ecuadorian university students. The overall prevalence of MetS in
our study, at 7.7%, was also greater than that in other Latin American countries such as Chile at 4.9%
and Argentina at 4.1% [35,36]. Clearly, the prevalence of MetS could differ between studies depending
on the MetS cluster used, the design method, and the target population. In this study, we used the IDF
and AHA/NHLBI [2] joint statement, as it was an international attempt to harmonize the definition of
MetS; central obesity is not an obligatory component of this definition and it is ethnic-specific.
Of those components, abdominal obesity, the most prevalent manifestation of MetS, is a marker
of dysfunctional adipose tissue, and is of central importance in clinical diagnosis [3741]. Our results
show correlation between BF%, FMI, and all of the cardiometabolic biomarkers analyzed, including
mean arterial pressure, glucose, HDL-C, LDL-C, triglycerides, and total cholesterol (<0.05 for all).
These findings agree with Knowles et al. [19], who studied a population of young Peruvian adults and
found significant correlations between the fat parameters and the above-mentioned cardiometabolic
biomarkers. Blood lipid disorders and adipose tissue are the key etiologic defects that define MetS;
we found all fat indices used in this study were associated with BF%. In contrast, other researchers
such as Schuster et al. [40], who studied a sample of 444 young adults in Brazil, only found correlations
between the BF% and glucose, HDL-C, and triglycerides. Our result may be different due to degree
and the prevalence varying on the basis of ethnicity, genetic susceptibility, lifestyle, and geographic
location. In addition, our results showed lower values of weight, height, and WC in women compared
to men. This aligns with Liu et al. [17], who studied a population of 1698 adults in China. In all
likelihood, these differences in body composition were due to sexual dimorphism [31] and diet [34].
Sex-specific hormones are another possible explanation. For example, the triglyceride levels and blood
pressure were also lower among women in comparison to men. In this context, much of the risk of
MetS associated with sex can be explained by the change in steroid hormone levels and the metabolism
Nutrients 2017, 9, 1009 9 of 13

of carbohydrates and lipids [39]. An increase in total fat and the distribution of central fat, resulting
from alterations in biomarker-disease, such as fasting glucose, triglycerides, and ferritin, which are
mediators of MetS, has been reported in female Hispanic/Latino adults [40]. This coincides with
previous research, in which this finding was correlated with lower cardiovascular morbidity and
dysfunctional adipose tissue in women [39,41]. Furthermore, the observation of ongoing changes
in body composition by sex and its relationship with obesity has demonstrated that obesity affects
individuals no matter their muscle mass, fat mass, height, and weight [41].
The AUC values for the MetS ROC analyses, at 0.835 for men and 0.838 for women, indicate that
BF% has moderate diagnostic capabilities to identify subjects with MetS (3 risk factors). Interestingly,
when considering MetS in our study, FMI showed the greatest AUC to predict MetS risk in women
compared to men. Results show that metabolic disorders are present in young adult independent of
age, smoking, physical activity, or fitness levels [42]. There is a growing interest in suggesting cut-off
points for body fat levels for the early detection of CVD risk. Future longitudinal studies should be
carried out to understand the role of different levels of adiposity on CVD risk stratification within
a college population.
In contrast, another study carried out by Mohammadreza et al. [43] among Iranian adults found
that BF% was not as effective a parameter for predicting MetS as other anthropometric indexes such
as BMI, waist-to-height ratio, and waist-to-hip ratio. In this same line, Mousa et al. [44] studied
a population of young adults and found that the predictive power of BF% and BMI for screening
MetS was limited. This discrepancy in results could be explained by the heterogeneity of the sample
populations. Consequently, the applicability and usefulness of BF% and FMI in the prediction of MetS
require further studies of different populations and ethnic groups. These results are partially consistent
with previous studies that showed BF% was positively correlated with single metabolic risk factors,
such as BMI and triglycerides, and negatively correlated with HDL cholesterol in men, but not in
women [45,46].
To our knowledge, few studies have explored the use of FMI as a proxy of obesity. In a study of
538 Mexican American college students (373 women and 165 men), the validity of FMI and BMI against
BF% with BIA as the reference method was evaluated [47]. Correlations between FMI and BF% resulted
in correlation coefficients of 0.976 in men (p < 0.001) and 0.992 in women (p < 0.001). However, similar
to our findings, the correlations between FMI and PBF were higher (r = 0.960, p < 0.01). In a study of
2986 healthy white men and 2649 white women, age 15 to 98 years in Switzerland, the mean FMI in
the overall age group was 4.9 (1.8) kg/m2 in men and 6.6 (2.4) kg/m2 in women [48], compared to our
results, of 6.6 (3.1) kg/m2 in men and 11.2 (3.4) kg/m2 in women without MetS. This difference can be
explained by the fact that FMI cutoffs in the Swiss group were derived from BMI and not from MetS
cutoffs. On the other hand, in the Peltz et al. study [47], the median FMI in the overall age group was
7.3 (interquartile range 4.5) kg/m2 in men and 9.0 (interquartile range 5.9) kg/m2 in women. Our FMI
means fell within the lower range of the Mexican American normal FMI ranges in both men and women.
This was expected, as South Americans have a lower percentage of body fat across all age groups when
compared to non-Hispanic whites, Mexican Americans, and non-Hispanic blacks [49]. In a subsequent
study from the same group (5635 apparently healthy adults from a mixed non-randomly selected
Caucasian population) in Switzerland, obesity was defined as an FMI greater than 8.2 kg/m2 in men
and 11.8 kg/m2 in women [50], which are similar than our FMI cutoffs of 6.9 kg/m2 in men and
11.8 kg/m2 in women in our study. These findings, although limited, show an interesting agreement
with our results, which collectively contribute to the concept of developing one set of recommended
ranges that are not affected by height.
Our results have public health and clinical implications as college populations have been reported
as a period in life when several behavioral and metabolic changes occur. These changes, in addition
to the adoption of a Western lifestyle and diet, have led to a rise in the prevalence of overweight
and obese Colombians, particularly among university students [32,51]. Further studies are needed to
Nutrients 2017, 9, 1009 10 of 13

identify clinical characteristics in young adults that could be used in screening tests to predict MetS
risk in adulthood.
The principal limitation of this study was the use of cross-sectional data. Furthermore, it is also
true that the hydration status of the participants could have modified the results of the BF% measured
with BIA. Most BIA prediction equations assume that the fat mass and fat-free mass consist of 73%
water [52]. These major limitations of the BIA method remain unresolved. Secondly, the assessment of
other biomarkers, such as insulin, adiponectin, and c-reactive protein levels, which could have shown
additional information about prognostic assessment, was not performed. These and other questions
deserve further investigation by future well-designed longitudinal studies.
The main strength of our study is the fact that our study compared the predictive power of both
BF% and FMI while providing cutoff values for the prediction of MetS in university students from
Colombia. Considering the wide use of BIA methods and their extension to assess body composition,
our study has important implications for evaluating CVD and metabolic risks in high-risk subjects,
such as those with MetS.

5. Conclusions
In conclusion, BF% and FMI had a moderate discriminatory power in the identification of MetS
in Colombian university students. Apart from the differences between our cut-off points and those
reported in other research in geographically different populations, this study reports the first cutoff
points for identification of MetS by BF% and FMI in Colombian young adults. We demonstrated that
a BF% 38.9% in women and 25.5% in men, and an FMI 11.8 kg/m2 in women and 6.9 kg/m2 in
men, are thresholds that could be used to predict Colombian young adults at high risk of MetS.

Acknowledgments: This study was part of the project entitled Body Adiposity Index and Biomarkers
of Endothelial and Cardiovascular Health in Adults, which was funded by Centre for Studies on Measurement of
Physical Activity, School of Medicine and Health Sciences, Universidad del Rosario (Code N FIUR DN-BG001),
and Universidad de Boyac (Code N RECT 60). The funder had no role in the study design, data collection,
data analysis and interpretation, the preparation of the manuscript, or the decision to publish.
Author Contributions: Robinson Ramrez-Vlez, Jorge Enrique Correa-Bautista, Alejandra Sanders-Tordecilla,
Mnica Liliana Ojeda-Pardo, Elisa Andrea Cobo-Meja, and Roco del Pilar Castellanos-Vega conceived and
designed the study; Antonio Garca-Hermoso, Emilio Gonzlez-Jimnez, Jacqueline Schmidt-RioValle contributed
to the data analysis; Katherine Gonzlez-Ruz analyzed the data and wrote the paper. All authors read and
approved the final manuscript.
Conflicts of Interest: The authors declare no conflict of interest.

Abbreviations
The following abbreviations are used in this manuscript:

BF body fat
BIA bioelectrical impedance analysis
BMI body mass index
CI confidence interval
CT computed tomography
CVD cardiovascular disease
DXA dual-energy x-ray absorptiometry
FUPRECOL association between muscular strength and metabolic risk factors in colombia
FMI fat mass index
HDL-C high-density lipoprotein cholesterol
IDF international diabetes federation
LDL-C low-density lipoprotein cholesterol
MetS metabolic syndrome
MRI magnetic resonance imaging
Nutrients 2017, 9, 1009 11 of 13

PA physical activity
SD standard deviation
WC waist circumference
WHO World Health Organization

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